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Repairing Fetal Membranes with a Self-Adhesive Ultrathin Polymeric Film: Evaluation in Mid-Gestational Rabbit Model

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Repairing Fetal Membranes with a Self-Adhesive Ultrathin Polymeric Film: Evaluation in Mid-Gestational Rabbit Model This is a repository copy of Repairing Fetal Membranes with a Self-adhesive Ultrathin Polymeric Film: Evaluation in Mid-gestational Rabbit Model. White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/105542/ Version: Accepted Version Article: Pensabene, V orcid.org/0000-0002-3352-8202, Patel, PP, Williams, P et al. (4 more authors) (2015) Repairing Fetal Membranes with a Self-adhesive Ultrathin Polymeric Film: Evaluation in Mid-gestational Rabbit Model. Annals of Biomedical Engineering, 43 (8). pp. 1978-1988. ISSN 0090-6964 https://doi.org/10.1007/s10439-014-1228-9 (c) Biomedical Engineering Society 2014. This is an author produced version of a paper published in the Annals of Biomedical Engineering. Uploaded in accordance with the publisher's self-archiving policy. 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[email protected] https://eprints.whiterose.ac.uk/ TITLE PAGE Title: Repairing fetal membranes with a self-adhesive ultrathin polymeric film: evaluation in mid-gestational rabbit model Authors: Virginia Pensabene1, PhD, Premal P Patel 1, Phillip Williams2, Assoc. Prof., Trisha L. Cooper3, MSM PA-C, Kellye C. Kirkbride1, PhD, Todd D. Giorgio1, Prof., Noel Tulipan3, Prof. 1Department of Biomedical Engineering, Vanderbilt University, Nashville, TN, USA 2Department of Surgery, Vanderbilt University Medical Center, Nashville, TN, USA 3Department of Pediatric Neurosurgery, Monroe Carrell Jr Children’s Hospital at Vanderbilt, Nashville, TN, USA Abbreviated title: Self-adhesive ultrathin film to repair fetal membranes Corresponding author: Virginia Pensabene, Department of Biomedical Engineering Vanderbilt University 5824 Stevenson Center, Nashville, TN (USA) 37235-1592 e-mail: [email protected] Phone: +1 615 525 7253, Fax: +1 615 343 7919 Abstract Preterm premature rupture of membranes (PPROM) causes 40% of all preterm births, affecting 150,000 women each year in the United States. Prenatal diagnostic procedures and surgical interventions increase incidence of adverse events, leading to iatrogenic membrane rupture after a fetoscopic procedure in 45% of cases. We propose an ultrathin, self-adherent, poly-L-lactic acid patch (“nanofilm”) as a reparative wound closure after endoscopic/fetoscopic procedures. These nanofilms are compatible with application in wet conditions and with minimally invasive instrumentation. Ex vivo studies to evaluate the nanofilm were conducted using human chorion-amnion (CA) membranes. A custom-built inflation device was used for mechanical characterization of CA membranes and for assessment of nanofilm adhesion and sealing of membrane defects up to 3 mm in size. These ex vivo tests demonstrated the ability of the nanofilm to seal human CA defects ranging in size from 1 to 3 mm in diameter. In vivo survival studies were conducted in 25 mid-gestational rabbits, defects were created by perforating the uterus and the CA membranes and subsequently using the nanofilm to seal these wounds. These in vivo studies confirmed the successful sealing of defects smaller than 3 mm observed ex vivo. Histological analysis of whole harvested uteri 7 days after surgery showed intact uterine walls in 59% of the nanofilm repaired fetuses, along with increased uterine size and intrauterine development in 63% of the cases. In summary, we have developed an ultrathin, self-adhesive nanofilm for repair of uterine membrane defects. Keywords Fetal surgery, IPPROM, amnion, chorion, ultrathin polymeric film, poly L-lactic acid 2 Introduction Fetal membranes (the chorion and the amnion) develop immediately after embryo implantation at six days of gestation. The fetal membrane continues to grow and change during the entire pregnancy protecting the fetus during its development inside the uterus. After 12 weeks of gestation, the amnion is clearly distinguishable from the chorion as a thin layer of epithelial cells in direct contact with the amniotic fluid. The chorion is a thicker membrane that is in close contact with the decidual layers and the endometrial tissue and at this stage is considered part of the placenta. The human fetal membranes are not innervated and the chorion is poorly vascularized. These membranes remain intact until the end of the pregnancy when estradiol secretion from the placenta stimulates the uterus to produce more oxytocin receptors and to release prostaglandins, which initiates uterine contractions and triggers mechanical fetal membrane rupture. The natural rupture of these membranes is part of the sequence of term delivery. Serious complications occur when fetal membrane rupture occurs prior to term. In 3% of all pregnancies, the membranes rupture prior to term, causing as many as 40% of all preterm births (1). Intrauterine rupture of the chorion-amnion (CA) membrane in the first three months of pregnancy (generally resulting in a miscarriage) can be distinguished from preterm premature rupture of the membrane (PPROM) which occurs when the CA membrane mechanically fails prior to the completion of 37 weeks of gestation. PPROM affects 150,000 women per year in the United States (2). Prenatal diagnostic procedures, such as chorion villi sampling and amniocentesis, and prenatal surgical interventions are currently possible. These procedures, however, significantly increase the incidence of adverse events and can often lead to iatrogenic membrane rupture (IPPROM). Prenatal rupture of the fetal membranes was found to occur after a fetoscopic procedure in 45% of cases (3, 4). The natural mechanism of repairing and sealing the fetal membranes is described as retraction, sliding, contraction and/or scarring in the myometrial and decidual layers of the uterus without involving inflammation, scar formation, and tissue regeneration (5). A fundamental reason for poor outcomes of existing techniques for repairing fetal membrane ruptures is based on the requirement for an active response by the tissue. Attempts to suture these unique membranes using bioactive sealants (such as injectible fibrin or collagen-based sealants) have been studied, but remain to be confirmed using consistent animal models (3). In fact, in most cases the mechanical properties of current materials do not match the mechanical characteristics of the fetal membranes due to the fact that they change continuously during gestation. For example, the application of sealant preparations containing blood components (such as fibrin, thrombin, fibrinogen, or platelets) was shown in human trials to prolong pregnancy, but a significant perinatal mortality rate (70%) remained. Extracellular matrix, maternal blood or collagen plugs have been compared in rabbit models in vivo and do not show significant improvements in the closure of fetoscopy access sites. Laser welding has been limited by heterogeneous thermal properties of the tissues as well as by the risk of thermal injury to the membranes. Finally, single synthetic components that self- polymerize to form a biocompatible hydrogel have been shown to restore the amniotic epithelial continuity, allowing compression and contraction of the tissue in the chorion layer. A recent review reported the diameter of the surgical instruments and the number of entries into the uterine cavity as the two main factors leading to IPPROM (6). Physical access and time constraints are critical to successful suturing of fetal tissues. Therefore, a primary goal of repair mechanisms is to reduce the duration and invasiveness of the surgical intervention as much as possible. In addition, the method used to suture the wound must not hinder the development of the fetus; therefore, the repair mechanism must be non-toxic, rapidly bioabsorbed, of minimal size, easily applied and adherent to the uterus. 4 To solve these current problems, we have developed an innovative ultrathin polymeric self-adherent patch as a repair method to use during fetal surgeries and invasive endoscopic/fetoscopic procedures. The methodology was developed to provide efficient, non- disruptive, non-toxic bonding to fetal membranes and to be compatible with deployment in wet conditions and with minimally invasive tools. The principal innovative aspect of these ultrathin films (also called “nanofilms”) compared to existing materials and techniques is their self-adhesive properties. The patch does not require glue or clips to adhere to wet surfaces since adhesion is primarily due to the nanometric thickness of the patch and secondarily to the polymeric composition of the film. Previous studies from the laboratory of Shinji Takeoka demonstrate excellent sealing efficacy of a poly-L-lactic acid (PLLA) nanofilm for gastric incisions as a novel wound dressing
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